Available online at www.sciencedirect.
com
Hormone balance and abiotic stress tolerance in crop plants
Zvi Peleg and Eduardo Blumwald
Plant hormones play central roles in the ability of plants to
adapt to changing environments, by mediating growth,
development, nutrient allocation, and source/sink transitions.
Although ABA is the most studied stress-responsive hormone,
the role of cytokinins, brassinosteroids, and auxins during
environmental stress is emerging. Recent evidence indicated
that plant hormones are involved in multiple processes. Cross-
talk between the different plant hormones results in synergetic
or antagonic interactions that play crucial roles in response of
plants to abiotic stress. The characterization of the molecular
mechanisms regulating hormone synthesis, signaling, and
action are facilitating the modification of hormone biosynthetic
pathways for the generation of transgenic crop plants with
enhanced abiotic stress tolerance.
Address
Department of Plant Sciences, University of California, Davis, CA 95616,
USA
Corresponding author: Blumwald, Eduardo (eblumwald@ucdavis.edu)
Current Opinion in Plant Biology 2011, 14:290–295
This review comes from a themed issue on
Physiology and metabolism
Edited by Ute Krämer and Anna Amtmann
Available online 4th March 2011
1369-5266/$ – see front matter
# 2011 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2011.02.001
Introduction
As sessile organisms, plants must regulate their growth
and development in order to respond to numerous external
stimuli and an ever-changing environment [1]. These
adaptations include the responses to temperature fluctu-
ations, water and nutrients imbalance, and pathogens, etc.
These responses are mediated by plant growth regulators
(phytohormones), compounds derived from plant biosyn-
thetic pathways that can act either at the site of synthesis or
following their transport, elsewhere in the plant. Collec-
tively, plant hormones regulate every aspect of plant
growth and development and the responses of plants to
biotic and abiotic stresses. Plant growth regulators include
the five classical phytohormones: abscisic acid (ABA),
ethylene, cytokinin (CK), auxin (IAA), gibberellin (GA),
jasmonate (JA), as well as brassinosteroids (BR), salicylic
acid (SA), nitric oxide (NO), and strigolactone (SL), and it
is likely that additional growth regulators are yet to be
discovered. In recent years, significant research progress
Current Opinion in Plant Biology 2011, 14:290–295
contributed to the understanding of processes associated
with the biosynthesis of plant hormones, their metabolism,
as well as their role in signaling. Studies using plants
bearing mutations in hormone-biosynthetic pathways have
been instrumental in advancing our understanding of the
processes associated with the plant responses to changing
environments. However, hormones do not act in isolation
but are interrelated by synergistic or antagonistic cross-talk
so that they modulate each other’s biosynthesis or
responses. Reviews on hormone action and signaling of
ABA [2–4], CK [5–7], ethylene [8], BR [9,10] and JA [11],
and on hormone cross-talk [12,13] have been published
recently. Here, we highlight the latest advances in our
understanding of the role of hormones and hormone cross-
talk in plant responses to abiotic stresses. We then discuss
the recent progress in the engineering of hormone-associ-
ated genes aimed at improving crop stress tolerance.
Hormones and the response to abiotic stress
Phytohormones are essential for the ability of plants to
adapt to abiotic stresses by mediating a wide range of
adaptive responses [13–15,16]. They often rapidly alter
gene expression by inducing or preventing the degradation
of transcriptional regulators via the ubiquitin–proteasome
system [17]. One of the most studied topics in the response
of plants to abiotic stress, especially water stress, is ABA
signaling and ABA-responsive genes. ABA synthesis is one
of the fastest responses of plants to abiotic stress, triggering
ABA-inducible gene expression [18] and causing stomatal
closure, thereby reducing water loss via transpiration [19]
and eventually restricting cellular growth. Numerous
genes associated with ABA de novo biosynthesis and genes
encoding ABA receptors and downstream signal relays
have been characterized in Arabidopsis thaliana (reviewed
by [2]). At least ten viviparous mutants have been
identified in maize (Zea mays), most of which (vp2, vp5,
vp7, vp9, w3, y3, and y9) were blocked in the biosynthesis of
the carotenoid precursors for de novo ABA synthesis. In rice
(Oryza sativa), four phs mutants, defective in phytoene
desaturase (OsPDS), z-carotene desaturase (OsZDS),
carotenoid isomerase (OsCRTISO), and lycopene b-cyclase
(b-OsLCY) were found to impact on the biosynthesis of
carotenoid precursors of ABA [20]. ABA also plays an
important role during plant adaptations to cold tempera-
tures. Cold stress induces the synthesis of ABA and the
exogenous application of ABA improves the cold tolerance
of plants [21]. Other hormones, in particular CK, SA,
ethylene, and JA, also play substantial direct or indirect
roles in the response of plants to abiotic stress. CK is an
antagonist to ABA, and the exposure of plants to water
limiting conditions results in decreased levels of CK.
Examination of public microarray expression data for
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 Hormone balance and abiotic stress tolerance in crop plants Peleg and Blumwald 291
A. thaliana revealed numerous genes encoding proteins
associated with CK signaling pathways that were differen-
tially affected by various abiotic stresses [14]. BR was
reported (mainly based on the exogenous application of
BR) to induce the expression of stress-related genes,
leading to the maintenance of photosynthesis activity,
the activation of antioxidant enzymes, the accumulation
of osmoprotectants, and the induction of other hormone
responses [10]. The overlap between hormone-regulated
gene suites during the adaptive responses of plants to
environmental stresses suggests the existence of a complex
network with extensive cross-talk between the different
hormone signaling pathways.
Hormone cross-talk
Evidence supporting hormone cross-talk comes mainly
from analysis of A. thaliana mutant phenotypes [13]. The
synergistic or antagonistic hormone action and the coor-
dinated regulation of hormone biosynthetic pathways play
crucial roles in the adaptation of plants to abiotic stress.
Recently, the role of auxins in drought tolerance was
postulated; TLD1/OsGH3.13, encoding indole-3-acetic
acid (IAA)-amido synthetase, was shown to enhance
the expression of LEA (late embryogenesis abundant)
genes, which correlated with the increased drought tol-
erance of rice seedlings [22]. The expression of many
other genes associated with auxin synthesis, perception,
and action has been shown to be regulated by ethylene
[8]. Among them, are the auxin-responsive factors ARF2
and ARF19 [23,24], the auxin transporters PIN1, PIN2,
PIN4, AUX1 [25], and genes encoding auxin biosynthetic
enzymes (ASA1/WEI2/TIR7, ASB1/WEI7, TAA1/SAV3/
WEI8) [26,27]. Conversely, auxin was found to affect
ethylene biosynthesis. Several members of the 1-amino-
cyclopropane-1-carboxylate synthase (ACS) gene family,
encoding rate-limiting enzymes in ethylene biosyn-
thesis, were shown to be regulated by auxin treatment
[28]. Recently, CK was also shown to be a positive
regulator of auxin biosynthesis, and it was postulated that
a homeostatic feedback regulatory loop involving both
CK and IAA signaling acts to maintain appropriate CK
and IAA concentrations in developing root and shoot
tissues [29]. GA and BR regulate many common phys-
iological processes. OsGSR1, a member of the GAST
(GA-stimulated transcript) gene family, was found to play
key roles in both BR and GA signaling pathways, and to
mediate the interaction between them [16]. RNAi trans-
genic rice plants with reduced OsGSR1 expression dis-
played phenotypes similar to plants deficient in BR,
including short primary roots, erect leaves and reduced
fertility. GA is also associated with SA. The exogenous
application of GA (GA3) induced increased expression
levels of ICS1 (isochorismate synthase1) and NPR1 (nonex-
pressor of pathogenesis related genes 1), genes involved in SA
biosynthesis and SA action, respectively [30]. Transgenic
A. thaliana plants constitutively overexpressing a GA-
responsive gene from Fagus sylvatica encoding FsGASA4,
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a member of the GA3 gene family, showed improved
tolerance under abiotic stress and the stress tolerance was
correlated with increased endogenous levels of SA [30].
ABA regulates stomatal opening during stress, however,
recent studies suggest that other hormones such as CK,
ethylene, BR, JA, SA, and NO also affect stomatal function
(reviewed by [31]). While ABA, BR, SA, JA, and NO induce
stomatal closure, CK and IAA promote stomatal opening.
NO operates as a key intermediate in the ABA-mediated
signaling network that regulates stomatal closure [32].
ABA is also a regulator of strigolactones biosynthesis, as
shown using tomato ABA-deficient mutants of different
steps in the ABA biosynthetic pathway and specific inhibi-
tors for different carotenoid cleaving enzymes [33].
Recently our own work has shown that expression of
IPT (isopentenyl transferase, a gene encoding a key step in
the biosynthesis of CK) under the control of a drought-
inducible and senescence-inducible promoter (PSARK) in
tobacco (Nicotiana tabacum) and rice results in a significant
alteration of gene expression associated with hormone
biosynthesis, response, and regulation [34,35]. Trans-
genic tomato (Solanum lycopersicum) rootstocks expressing
IPT had enhanced root CK synthesis that was shown to
modify shoot hormonal balance under salinity stress [36].
The PSARK<IPT tobacco and rice plants showed an upre-
gulation of BR-biosynthesis and BR-regulation and
signaling genes, suggesting an interaction between CK
and BR [34,35]. BR-mediated signaling was regulated
by ABA through BIN2 or its upstream components via the
PP2C ( protein phosphatase 2C) family of genes [37]. ABA
was also shown to inhibit BR-induced responses during
the exposure of plants to abiotic stress [38]. Whether the
positive interaction between CK and BR is a consequence
of direct cross-talk between CK and BR or indirectly
mediated by ABA remains unclear at this stage [34].
Biotechnological applications
A large number of genes associated with de novo ABA
biosynthesis and genes encoding ABA receptors and
downstream signal relays have been characterized in
Arabidopsis (reviewed by [2]). The catalytic steps of
ABA biosynthesis involving the conversion of b-carotene
to ABA is mediated by the action of enzymes encoded by
ABA1/LOS6, ABA4, NCED, ABA2, and ABA3/LOS5 [39].
Some of these genes have been manipulated in crops.
ABA3/LOS5 encodes a Mo-cofactor sulfurase (MCSU)
that catalyzes the final conversion of abscisic aldehyde to
ABA. The expression of ABA3/LOS5 was enhanced when
A. thaliana plants were exposed to drought or salt [40].
Overexpression of ABA3/LOS5 under the control of con-
stitutive or drought-inducible promoters resulted in a
significant increase in transgenic rice yield under drought
conditions in the field [41]. NCED encodes 9-cis-epoxy
carotenoid dioxygenase, an enzyme that catalyzes the
conversion of neoxanthin to xanthoxin, a rate-limiting
reaction in the synthesis of ABA. In A. thaliana, AtNCED3
Current Opinion in Plant Biology 2011, 14:290–295
292 Physiology and metabolism
plays a crucial role in drought-stress-inducible ABA
biosynthesis, and T-DNA insertional nced3 mutants have
defects in ABA accumulation under drought stress and
impaired drought tolerance. Tobacco plants constitu-
tively overexpressing SgNCED1 (from Stylosanthes guia-
nensis) displayed a 51–77% increase in leaf ABA
accumulation, which resulted in enhanced tolerance of
the transgenic plants to drought and salinity [42]. The
transgenic NCED1 plants were similar in size to the wild-
type plants, and under drought they were able to maintain
relative growth rates similar to that of the wild-type plants
under normal conditions. The constitutive overexpres-
sion of LeNCED1 in tomato also resulted in increased
ABA accumulation in the transgenic plants [43]. Under
well-watered conditions, the transgenic plants showed a
reduction in assimilation rates, leaf chlorosis. Under
water-deficit conditions, these effects did not reduce
biomass production, presumably because of counteract-
ing positive effects of ABA on leaf expansion through
improved water status [43]. The modification of genes
involved in the regulation of the plant responses to ABA
is an alternative approach to enhance of plant stress
resistance. ERA1 encodes the b-subunit of farnesyltrans-
ferase, an enzyme associated with ABA-dependent signal
transduction [44]. Transgenic canola (Brassica napus L.)
carrying an era1 antisense construct driven by the
drought-inducible rd29A promoter from A. thaliana dis-
played enhanced yield under a mild drought stress [45].
CK is an antagonist to ABA, and the exposure of plants to
drought results in decreased levels of CK. Elevated CK
levels promoted survival under water-stress conditions,
inhibited leaf senescence and induced increased proline
Figure 1
Well watered, control
Wild type
Effects of water-stress on growth of rice (Oryza sativa) plants. Wild-type (WT) and transgenic plants expressing PSARK<IPT grown under well-watered
conditions and plants subjected to water-stress at pre-anthesis follow re-watering as described [34].
Current Opinion in Plant Biology 2011, 14:290–295
levels [46]. Manipulation of endogenous CK levels was
effective in delaying senescence. The IPT gene has been
overexpressed in several plant species under different
promoters and the transgenic plants were tested for
tolerance to various environmental stresses (reviewed
by [47]). The constitutive overexpression of IPT
increased endogenous CK concentrations up to 150-fold
and resulted in decreased root growth and in water stress
[48]. The use of inducible promoters for the conditional
expression of hormone biosynthentic genes makes it
possible to control hormone levels without the negative
effects on growth and development produced by very
large changes in hormone concentrations. The senes-
cence-induced promoter PSAG12 [49] has been used to
drive the IPT expression, resulting in a significant delay in
plant senescence. However, a significant delay in flower-
ing and reduced yield were also observed (reviewed by
[47]), probably due to altered source/sink relationships
brought about by the lack of chlorophyll and protein
degradation in source leaves [50]. The use of matu-
ration-induced and stress-induced promoters (SARK,
senescence associated receptor kinase [50]) to drive IPT
expression in both dicots and monocots provided an
alternative approach for the induction of IPT and the
concomitant biosynthesis of CK, without the negative
effects of constitutively high CK content on plant
phenology (i.e. flowering time, plant architecture, etc.)
[34,35,50,51]. IPT was expressed in the whole plant,
its maximal expression was attained during the drought
episode and the transgenic plants displayed enhanced
drought tolerance and superior yields (Figure 1) [34].
Tomato plants grafted onto rootstocks constitutively
water stress at reproductive stage
Wild type SARK::IPT
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 Hormone balance and abiotic stress tolerance in crop plants Peleg and Blumwald 293
expressing IPT resulted in a decrease of root biomass under
control conditions. However, under salinity-stress con-
ditions the transgenic plants yielded 30% more than the
wild type plants [36]. An alternative approach to intro-
ducing the IPT gene is to fuse IPT to the 30 end other genes
under the control of a single constitutive promoter. The
distance of the IPT gene from the constitutive promoter
resulted in a moderate IPT expression and only a 2–3 fold
increase of CK levels. This resulted in improved stress
tolerance in transgenic plants [52], supporting the notion
that moderate increases in CK can be an effective strategy
for improving stress tolerance. Exogenous application of
BRs was reported in diverse plant species to induce
drought tolerance [38]. Nevertheless, using BR-deficient
mutant it was shown that endogenous BRs or perception of
the same are not required for plants to respond to water
stress [53]. The overexpression of AtDWF4, a gene
involved in BR biosynthetic, under the control of a
seed-specific oleosin promoter resulted in improved germi-
nation of seeds that were previously treated with ABA,
which suggests an antagonic effect of BR on ABA-
regulated processes. Furthermore transgenic seedlings
were more tolerant to cold stress than wild-type seedlings
[54]. A knockout T-DNA insertion mutant of Osgsk1 (a rice
GSK3/SHAGGY-like protein kinase gene, ortholog of AtBIN2/
AtSK21, a negative regulator of BR-signaling), showed
greater tolerance to abiotic stresses, while OsGSK1 over-
expression in Arabidopsis resulted in stunted growth [55].
Antagonism between BR and ABA was recently demon-
strated in transgenic PSARK<IPT rice plants, where the
increase in CK induced BR-associated genes and repressed
ABA-related processes [34]. These results further high-
light the importance of hormone cross-talk during the
response of plants to abiotic stress.
Conclusions
The molecular mechanisms regulating hormone synthesis,
signaling, and action have been elucidated during the past
few years, and the roles of plant hormones for responses to
changing environments have been demonstrated. These
findings will facilitate the modification of hormone biosyn-
thetic pathways for the generation of transgenic plants with
enhanced abiotic stress tolerance. Controlling the hormone
dose/response ratio remains a challenge, since the hormone
levels attained should be moderate in order to maintain a
balance between the positive effects of plant hormones on
stress tolerance and the negative effects on growth and
development. The use of conditional promoters driving
gene expression at specific developmental stages, in
specific tissues/organs and/or in response to specific
environmental cues circumvents this problem and will
facilitate the generation of transgenic crops able to grow
under various abiotic stresses with minimal yield losses.
Acknowledgements
We apologize to colleagues whose work could not be cited owing to space
limitations. The research in our lab was supported by grants from NSF-IOS-
www.sciencedirect.com
0802112, CGIAR GCP#3008.03, UC Discovery #bio06-10627, and the Will
W. Lester Endowment of University of California. Z.P. was supported by
Vaadia-BARD Postdoctoral Fellowship Award (FI-419-08) from the US-
Israel Binational Agricultural Research and Development Fund.
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